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(Carnian) of Brazil and the Rise of Sphenodontians in Gondwana Received: 30 November 2018 Annie S

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(Carnian) of Brazil and the Rise of Sphenodontians in Gondwana Received: 30 November 2018 Annie S www.nature.com/scientificreports OPEN A New Clevosaurid from the Triassic (Carnian) of Brazil and the Rise of Sphenodontians in Gondwana Received: 30 November 2018 Annie S. Hsiou 1, Randall L. Nydam2, Tiago R. Simões 3,4, Flávio A. Pretto5, Silvio Onary1, Accepted: 2 August 2019 Agustín G. Martinelli 6,7, Alexandre Liparini8, Paulo R. Romo de Vivar Martínez7, Published: xx xx xxxx Marina B. Soares7, Cesar L. Schultz7 & Michael W. Caldwell3,9 The early evolution of lepidosaurs is marked by an extremely scarce fossil record during the Triassic. Importantly, most Triassic lepidosaur specimens are represented by disarticulated individuals from high energy accretion deposits in Laurasia, thus greatly hampering our understanding of the initial stages of lepidosaur evolution. Here, we describe the fragmentary remains of an associated skull and mandible of Clevosaurus hadroprodon sp. nov., a new taxon of sphenodontian lepidosaur from the Late Triassic (Carnian; 237–228 Mya) of Brazil. Referral to Sphenodontia is supported by the combined presence of a marginal dentition ankylosed to the apex of the dentary, maxilla, and premaxilla; the presence of ‘secondary bone’ at the bases of the marginal dentition; and a ventrally directed mental process at the symphysis of the dentary. Our phylogenetic analyses recover Clevosaurus hadroprodon as a clevosaurid, either in a polytomy with the Late Triassic to Early Jurassic Clevosaurus and Brachyrhinodon (under Bayesian inference), or nested among diferent species of Clevosaurus (under maximum parsimony). Clevosaurus hadroprodon represents the oldest known sphenodontian from Gondwana, and its clevosaurid relationships indicates that these sphenodontians achieved a widespread biogeographic distribution much earlier than previously thought. Te Triassic period marks one of the great transitions in the history of life afer the mass-extinction at the end of the Permian. Most notably, this was a period of diversifcation of several major groups of extant terrestrial and marine vertebrates1, including lepidosaurian (Squamata + Rhynchocephalia) reptiles2. Today, Lepidosauria is the largest and the most diverse group of non-avian reptiles with over 10,000 known species3. Most of these are lizards and snakes with rhynchocephalians limited to two recognized sphenodontian species (Sphenodon punctatus and S. guntheri) in New Zealand4. However, during the early Mesozoic, rhynchocephalians (particularly sphenodon- tians), were the most diverse and widely distributed members of Lepidosauria5. In the last decade, the discovery of several important fossils has greatly increased our knowledge of the anat- omy, systematics, distribution, and early evolution of sphenodontians. Tese new fndings include presumably stem rhynchocephalians of the Late Triassic, such as Gephyrosaurus evansae6 and Penegephyrosaurus curtiscoppi7 from the United Kingdom, and Deltadectes elvetica7 from Switzerland. These three taxa, though not being well-understood phylogenetically, have been tentatively positioned as stem rhynchocephalians, sharing morpho- logical features with Gephyrosaurus and closely related taxa6,7. By far, the most well-known early sphenodontian clade is Clevosauridae, which currently includes several species allocated to three genera: Brachyrhinodon, Clevosaurus, and Polysphenodon from the Late Triassic to Early 1Laboratório de Paleontologia, Universidade de São Paulo, Ribeirão Preto, São Paulo, Brazil. 2Arizona College of Osteopathic Medicine and Department of Anatomy, College of Graduate Studies, Midwestern University, Glendale, AZ, 85308, USA. 3Department of Biological Sciences, University of Alberta, Edmonton, Canada. 4Present address: Department of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA, 02138, USA. 5CAPPA - Centro de Apoio à Pesquisa Paleontológica da Quarta Colônia, Universidade Federal de Santa Maria, São João do Polêsine, Brazil. 6CONICET-Sección Paleontología de Vertebrados, Museo Argentino de Ciencias Naturales ‘Bernardino Rivadavia’, Buenos Aires, Argentina. 7Laboratório de Paleontologia de Vertebrados, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil. 8PIBi-Lab – Laboratório de Pesquisas Integrativas em Biodiversidade, Departamento de Biologia, Universidade Federal de Sergipe, São Cristóvão, Sergipe, Brazil. 9Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, Canada. Correspondence and requests for materials should be addressed to A.S.H. (email: [email protected]) SCIENTIFIC REPORTS | (2019) 9:11821 | https://doi.org/10.1038/s41598-019-48297-9 1 www.nature.com/scientificreports/ www.nature.com/scientificreports Jurassic of Britain8–12, Germany9,13,14, Africa15,16, China17, North America18, and South America19. Although sup- port for this clade has not been universal9,20–22, the genus Clevosaurus is currently considered the most specious (six species) and widely distributed (Asia, Europe, North America, South America, Africa) of the clevosaurid taxa17,18,23–25. The new sphenodontian taxon described herein is the oldest unequivocal record of Rhynchocephalia (Sphenodontia) from South America, as well as in Gondwana. It provides the frst evidence of a greater diversity of early sphenodontians than previously understood for southern Pangaea and provides new information on the earliest stages of the acquisition of the acrodont dentition in sphenodontians in combination with unique dental specializations. Results Systematic Palaeontology. Lepidosauria Dumeril and Bibron, 1839 sensu Evans, 1984 Rhynchocephalia Gunther, 1867 sensu Gauthier et al., 1988 Sphenodontia Williston, 1925 sensu Benton, 1985 Referral to Sphenodontia is supported by the combined presence of a marginal dentition ankylosed to the apex of the dentary, maxilla, and premaxilla; the presence of “secondary bone” (sensu Harrison26,27, Fraser28 and Jones22) at the bases of the marginal dentition; a ventrally directed mental process (sensu Apesteguía29,30) at the symphysis of the dentary; presence of a very shallow Meckelian canal. Clevosauridae Bonaparte and Sues, 2006 (sensu this study) New defnition. Clevosauridae was originally defned by Bonaparte and Sues19 as the least inclusive clade containing the last common ancestor shared between Brachyrhinodon, Polysphenodon, and Clevosaurus plus all of its descendants. Due to the uncertain position of Polysphenodon (i.e. if the genus is or is not closely related to the sister group Brachyrhinodon + Clevosaurus) in other topologies9,20,21,25, here we adopt the interpretation of Clevosauridae as a monophyletic group using the node–based defnition of the clade containing the last common ancestor shared between Brachyrhinodon and Clevosaurus plus all of its descendants. Clevosaurus hadroprodon sp. nov. Etymology. Species epithet comes from a combination of ‘hadroprodon’ (from the Greek “hadros”-meaning large) and “protos”, meaning frst (Greek), and “odous”, meaning tooth (Greek); in reference to the “big frst tooth”, i.e. the large tusk-like tooth of the premaxilla and the anteriormost/frst dentary tooth position. Holotype. MMACR PV-027-T, an incomplete right premaxilla, an incomplete right maxilla and right lower jaw in occlusion, and lef lower jaw located below these elements. Referred material. MMACR PV-028-T, an incomplete lef lower jaw; and MMACR PV-029-T, fragment of dentary with three isolated teeth. Locality and horizon. Linha Bernardino locality, Candelária municipality, Rio Grande do Sul State, Southern Brazil (Fig. 1); Santa Maria Formation (Santa Maria Supersequence, Candelária Sequence), Rosário do Sul Group, Paraná Basin; Carnian, Late Triassic31,32 (Fig. 1a–c). Clevosaurus hadroprodon was recovered from immediately beneath the layers that contained the cranial and postcranial remains of the cynodonts Exaeretodon sp. and Trucidocynodon sp. and a distal portion of femur that closely resembles the early dino- saur cf. Pampadromaeus (Fig. 1b). Te presence of these fossils referred to Exaeretodon, Trucidocynodon and a Pampadromaeus-like form places this locality within the Hyperodapedon AZ at the base of the Candelária Sequence. Recent high-precision U-Pb zircon geochronology data recovered a weighted mean 206Pb/238U date of 233.23 ± 0.73 Ma for typical Hyperodapedon AZ sites33, which can be biostratigraphically correlated to the sedimentary layers containing C. hadroprodon. As such we conservatively consider the age for the fossil material to be Carnian (Late Triassic). Diagnosis. Small sphenodontian rhynchocephalian difering from all other known sphenodontians in pos- sessing the following combination of features: (1) a large, blunt, tusk-like tooth in both premaxilla and frst tooth position of dentary; (2) in having an angled, but nearly vertical mandibular symphysis and relatively deep den- tary; (3) absence of an edentulous gap between the tusk-like tooth and the remaining dentition; (4) absence of a posterodorsal process of the premaxilla; (5) in lacking well-developed medial-posteromedial expansion of the posterior dentition; (6) and lacking fanges on the teeth, and (7) lacking labially expanded teeth. Feature 4 makes this new taxon diferent from many sphenodontians, including other species of Clevosaurus, Rebbanasaurus, Godavariasaurus, Priosphenodon, Sphenotitan, Paminzisaurus and Ankylosphenodon. Features 5 and 6 make this taxon diferent from all other described species of Clevosaurus [Clevosaurus hudsoni, C. bairdi, C. latidens, C. sectumsemper, C. cambrica, and Clevosaurus
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